Testin interacts with vangl2 genetically to regulate inner ear sensory cell orientation and the normal development of the female reproductive tract in mice

Developmental Dynamics

Volumn 242, Issue 12, 2013, Pages 1454-1465

  Ren, Dong Dong ^a,b   Kelly, Michael ^b   Kim, Sun Myoung ^b   Grimsley Myers, Cynthia Mary ^b   Chi, Fang Lu ^a   Chen, Ping ^b  

^a FUDAN UNIVERSITY   (China)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Female reproductive tract; Hair cells; Inner ear; Planar cell polarity; Testin; Vangl2

Indexed keywords

CELL MEMBRANE PROTEIN; COMPLEMENTARY DNA; METHYLTESTOSTERONE; UNCLASSIFIED DRUG; VAN GOGH LIKE 2 PROTEIN;

ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL TISSUE; ARTICLE; AUDITORY ORIENTATION; CELL INTERACTION; CELL POLARITY; CELLULAR PARAMETERS; COCHLEA; CONTROLLED STUDY; DNA LIBRARY; FEMALE; FEMALE GENITAL SYSTEM; GENE ACTIVATION; GENE INTERACTION; GENETIC REGULATION; HAIR CELL; MOUSE; NONHUMAN; ORGANOGENESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN PROTEIN INTERACTION; SENSORY NERVE CELL; VAGINA; VESTIBULE;

MAMMALIA; MUS;

FEMALE REPRODUCTIVE TRACT; HAIR CELLS; INNER EAR; PLANAR CELL POLARITY; TESTIN; VANGL2;

ANIMALS; DNA-BINDING PROTEINS; EAR, INNER; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENITALIA, FEMALE; HISTOLOGICAL TECHNIQUES; MICE; MICROSCOPY, CONFOCAL; NERVE TISSUE PROTEINS; TWO-HYBRID SYSTEM TECHNIQUES;

EID: 84888050808     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.24042     Document Type: Article

References (66)

1. Ahmad-Annuar A, Ciani L, Simeonidis I, Herreros J, Fredj NB, Rosso SB, Hall A, Brickley S, Salinas PC. 2006. Signaling across the synapse: a role for Wnt and Dishevelled in presynaptic assembly and neurotransmitter release. J Cell Biol 174:127-139.
2. Ansley SJ, Badano JL, Blacque OE, Hill J, Hoskins BE, Leitch CC, Kim JC, Ross AJ, Eichers ER, Teslovich TM, Mah AK, Johnsen RC, Cavender JC, Lewis RA, Leroux MR, Beales PL, Katsanis N. 2003. Basal body dysfunction is a likely cause of pleiotropic Bardet-Biedl syndrome. Nature 425:628-633.
3. Armstrong A, Ryu YK, Chieco D, Kuruvilla R. 2011. Frizzled3 is required for neurogenesis and target innervation during sympathetic nervous system development. J Neurosci 31:2371-2381.
4. Banerjee S, Gordon L, Donn TM, Berti C, Moens CB, Burden SJ, Granato M. 2011. A novel role for MuSK and non-canonical Wnt signaling during segmental neural crest cell migration. Development 138:3287-3296.
5. Barrow JR. 2006. Wnt/PCP signaling: a veritable polar star in establishing patterns of polarity in embryonic tissues. Semin Cell Dev Biol 17:185-193.
6. Bekman E, Henrique D. 2002. Embryonic expression of three mouse genes with homology to the Drosophila melanogaster prickle gene. Mech Dev 119(Suppl 1):S77-S81.
7. Berger-Muller S, Suzuki T. 2011. Seven-pass transmembrane cadherins: roles and emerging mechanisms in axonal and dendritic patterning. Mol Neurobiol 44:313-320.
8. Boeda B, Briggs DC, Higgins T, Garvalov BK, Fadden AJ, McDonald NQ, Way M. 2007. Tes, a specific Mena interacting partner, breaks the rules for EVH1 binding. Mol Cell 28:1071-1082.
9. Carreira-Barbosa F, Concha ML, Takeuchi M, Ueno N, Wilson SW, Tada M. 2003. Prickle 1 regulates cell movements during gastrulation and neuronal migration in zebrafish. Development 130:4037-4046.
10. Chen P, Segil N. 1999. p27(Kip1) links cell proliferation to morphogenesis in the developing organ of Corti. Development 126:1581-1590.
11. Ciruna B, Jenny A, Lee D, Mlodzik M, Schier AF. 2006. Planar cell polarity signalling couples cell division and morphogenesis during neurulation. Nature 439:220-224.
12. Coutts AS, MacKenzie E, Griffith E, Black DM. 2003. TES is a novel focal adhesion protein with a role in cell spreading. J Cell Sci 116:897-906.
13. Curtin JA, Quint E, Tsipouri V, Arkell RM, Cattanach B, Copp AJ, Henderson DJ, Spurr N, Stanier P, Fisher EM, Nolan PM, Steel KP, Brown SD, Gray IC, Murdoch JN. 2003. Mutation of Celsr1 disrupts planar polarity of inner ear hair cells and causes severe neural tube defects in the mouse. Curr Biol 13:1129-1133.
14. Dai D, Zhu H, Wlodarczyk B, Zhang L, Li L, Li AG, Finnell RH, Roop DR, Chen J. 2011. Fuz controls the morphogenesis and differentiation of hair follicles through the formation of primary cilia. J Invest Dermatol 131:302-310.
15. Das G, Jenny A, Klein TJ, Eaton S, Mlodzik M. 2004. Diego interacts with Prickle and Strabismus/Van Gogh to localize planar cell polarity complexes. Development 131:4467-4476.
16. Deans MR, Antic D, Suyama K, Scott MP, Axelrod JD, Goodrich LV. 2007. Asymmetric distribution of prickle-like 2 reveals an early underlying polarization of vestibular sensory epithelia in the inner ear. J Neurosci 27:3139-3147.
17. Devenport D, Fuchs E. 2008. Planar polarization in embryonic epidermis orchestrates global asymmetric morphogenesis of hair follicles. Nat Cell Biol 10:1257-1268.
18. Dingwell KS, Smith JC. 2006. Tes regulates neural crest migration and axial elongation in Xenopus. Dev Biol 293:252-267.
19. Drusco A, Zanesi N, Roldo C, Trapasso F, Farber JL, Fong LY, Croce CM. 2005. Knockout mice reveal a tumor suppressor function for Testin. Proc Natl Acad Sci U S A 102:10947-10951.
20. Etheridge SL, Ray S, Li S, Hamblet NS, Lijam N, Tsang M, Greer J, Kardos N, Wang J, Sussman DJ, Chen P, Wynshaw-Boris A. 2008. Murine dishevelled 3 functions in redundant pathways with dishevelled 1 and 2 in normal cardiac outflow tract, cochlea, and neural tube development. PLoS Genet 4:e1000259.
21. Garvalov BK, Higgins TE, Sutherland JD, Zettl M, Scaplehorn N, Kocher T, Piddini E, Griffiths G, Way M. 2003. The conformational state of Tes regulates its zyxin-dependent recruitment to focal adhesions. J Cell Biol 161:33-39.
22. Griffith E, Coutts AS, Black DM. 2005. RNAi knockdown of the focal adhesion protein TES reveals its role in actin stress fibre organisation. Cell Motil Cytoskeleton 60:140-152.
23. Grimsley-Myers CM, Sipe CW, Geleoc GS, Lu X. 2009. The small GTPase Rac1 regulates auditory hair cell morphogenesis. J Neurosci 29:15859-15869.
24. Hamblet NS, Lijam N, Ruiz-Lozano P, Wang J, Yang Y, Luo Z, Mei L, Chien KR, Sussman DJ, Wynshaw-Boris A. 2002. Dishevelled 2 is essential for cardiac outflow tract development, somite segmentation and neural tube closure. Development 129:5827-5838.
25. Henderson DJ, Chaudhry B. 2011. Getting to the heart of planar cell polarity signaling. Birth Defects Res A Clin Mol Teratol 91:460-467.
26. Heydeck W, Zeng H, Liu A. 2009. Planar cell polarity effector gene Fuzzy regulates cilia formation and Hedgehog signal transduction in mouse. Dev Dyn 238:3035-3042.
27. Jenny A, Darken RS, Wilson PA, Mlodzik M. 2003. Prickle and Strabismus form a functional complex to generate a correct axis during planar cell polarity signaling. EMBO J 22:4409-4420.
28. Jenny A, Reynolds-Kenneally J, Das G, Burnett M, Mlodzik M. 2005. Diego and Prickle regulate Frizzled planar cell polarity signalling by competing for Dishevelled binding. Nat Cell Biol 7:691-697.
29. Jiang D, Munro EM, Smith WC. 2005. Ascidian prickle regulates both mediolateral and anterior-posterior cell polarity of notochord cells. Curr Biol 15:79-85.
30. Jones C, Chen P. 2008. Chapter eight primary cilia in planar cell polarity regulation of the inner ear. Curr Top Dev Biol 85:197-224.
31. Jones C, Roper VC, Foucher I, Qian D, Banizs B, Petit C, Yoder BK, Chen P. 2008. Ciliary proteins link basal body polarization to planar cell polarity regulation. Nat Genet 40:69-77.
32. Katoh M, Katoh M. 2003. Identification and characterization of human PRICKLE1 and PRICKLE2 genes as well as mouse Prickle1 and Prickle2 genes homologous to Drosophila tissue polarity gene prickle. Int J Mol Med 11:249-256.
33. Kelly M, Chen P. 2007. Shaping the mammalian auditory sensory organ by the planar cell polarity pathway. Int J Dev Biol 51:535-547.
34. Kibar Z, Vogan KJ, Groulx N, Justice MJ, Underhill DA, Gros P. 2001. Ltap, a mammalian homolog of Drosophila Strabismus/Van Gogh, is altered in the mouse neural tube mutant Loop-tail. Nat Genet 28:251-255.
35. Kramer-Zucker AG, Olale F, Haycraft CJ, Yoder BK, Schier AF, Drummond IA. 2005. Cilia-driven fluid flow in the zebrafish pronephros, brain and Kupffer's vesicle is required for normal organogenesis. Development 132:1907-1921.
36. Li S, Esterberg R, Lachance V, Ren D, Radde-Gallwitz K, Chi F, Parent JL, Fritz A, Chen P. 2011. Rack1 is required for Vangl2 membrane localization and planar cell polarity signaling while attenuating canonical Wnt activity. Proc Natl Acad Sci U S A 108:2264-2269.
37. Lu X, Borchers AG, Jolicoeur C, Rayburn H, Baker JC, Tessier-Lavigne M. 2004. PTK7/CCK-4 is a novel regulator of planar cell polarity in vertebrates. Nature 430:93-98.
38. Mericskay M, Kitajewski J, Sassoon D. 2004. Wnt5a is required for proper epithelial-mesenchymal interactions in the uterus. Development 131:2061-2072.
39. Montcouquiol M, Rachel RA, Lanford PJ, Copeland NG, Jenkins NA, Kelley MW. 2003. Identification of Vangl2 and Scrb1 as planar polarity genes in mammals. Nature 423:173-177.
40. Montcouquiol M, Sans N, Huss D, Kach J, Dickman JD, Forge A, Rachel RA, Copeland NG, Jenkins NA, Bogani D, Murdoch J, Warchol ME, Wenthold RJ, Kelley MW. 2006. Asymmetric localization of Vangl2 and Fz3 indicate novel mechanisms for planar cell polarity in mammals. J Neurosci 26:5265-5275.
41. Murdoch JN, Doudney K, Paternotte C, Copp AJ, Stanier P. 2001a. Severe neural tube defects in the loop-tail mouse result from mutation of Lpp1, a novel gene involved in floor plate specification. Hum Mol Genet 10:2593-2601.
42. Murdoch JN, Rachel RA, Shah S, Beermann F, Stanier P, Mason CA, Copp AJ. 2001b. Circletail, a new mouse mutant with severe neural tube defects: chromosomal localization and interaction with the loop-tail mutation. Genomics 78:55-63.
43. Park TJ, Haigo SL, Wallingford JB. 2006. Ciliogenesis defects in embryos lacking inturned or fuzzy function are associated with failure of planar cell polarity and Hedgehog signaling. Nat Genet 38:303-311.
44. Paudyal A, Damrau C, Patterson VL, Ermakov A, Formstone C, Lalanne Z, Wells S, Lu X, Norris DP, Dean CH, Henderson DJ, Murdoch JN. 2010. The novel mouse mutant, chuzhoi, has disruption of Ptk7 protein and exhibits defects in neural tube, heart and lung development and abnormal planar cell polarity in the ear. BMC Dev Biol 10:87.
45. Phillips HM, Murdoch JN, Chaudhry B, Copp AJ, Henderson DJ. 2005. Vangl2 acts via RhoA signaling to regulate polarized cell movements during development of the proximal outflow tract. Circ Res 96:292-299.
46. Qian D, Jones C, Rzadzinska A, Mark S, Zhang X, Steel KP, Dai X, Chen P. 2007. Wnt5a functions in planar cell polarity regulation in mice. Dev Biol 306:121-133.
47. Rotter B, Bournier O, Nicolas G, Dhermy D, Lecomte MC. 2005. AlphaII-spectrin interacts with Tes and EVL, two actin-binding proteins located at cell contacts. Biochem J 388:631-638.
48. Shafer B, Onishi K, Lo C, Colakoglu G, Zou Y. 2012. Vangl2 promotes Wnt/planar cell polarity-like signaling by antagonizing Dvl1-mediated feedback inhibition in growth cone guidance. Dev Cell 20:177-191.
49. Sheldahl LC, Slusarski DC, Pandur P, Miller JR, Kuhl M, Moon RT. 2003. Dishevelled activates Ca2+ flux, PKC, and CamKII in vertebrate embryos. J Cell Biol 161:769-777.
50. Shimizu K, Sato M, Tabata T. 2011. The Wnt5/planar cell polarity pathway regulates axonal development of the Drosophila mushroom body neuron. J Neurosci 31:4944-4954.
51. Sipe CW, Lu X. 2011. Kif3a regulates planar polarization of auditory hair cells through both ciliary and non-ciliary mechanisms. Development 138:3441-3449.
52. Terabayashi T, Funato Y, Fukuda M, Miki H. 2009. A coated vesicle-associated kinase of 104 kDa (CVAK104) induces lysosomal degradation of frizzled 5 (Fzd5). J Biol Chem 284:26716-26724.
53. Tissir F, Goffinet AM. 2010. Planar cell polarity signaling in neural development. Curr Opin Neurobiol 20:572-577.
54. Topczewski J, Dale RM, Sisson BE. 2011. Planar cell polarity signaling in craniofacial development. Organogenesis 7:255-259.
55. Torban E, Kor C, Gros P. 2004a. Van Gogh-like2 (Strabismus) and its role in planar cell polarity and convergent extension in vertebrates. Trends Genet 20:570-577.
56. Torban E, Wang HJ, Groulx N, Gros P. 2004b. Independent mutations in mouse Vangl2 that cause neural tube defects in looptail mice impair interaction with members of the Dishevelled family. J Biol Chem 279:52703-52713.
57. Tree DR, Shulman JM, Rousset R, Scott MP, Gubb D, Axelrod JD. 2002. Prickle mediates feedback amplification to generate asymmetric planar cell polarity signaling. Cell 109:371-381.
58. Vandenberg AL, Sassoon DA. 2009. Non-canonical Wnt signaling regulates cell polarity in female reproductive tract development via van gogh-like 2. Development 136:1559-1570.
59. Veeman MT, Slusarski DC, Kaykas A, Louie SH, Moon RT. 2003. Zebrafish prickle, a modulator of noncanonical Wnt/Fz signaling, regulates gastrulation movements. Curr Biol 13:680-685.
60. Wallingford JB. 2012. Planar cell polarity and the developmental control of cell behavior in vertebrate embryos. Annu Rev Cell Dev Biol 28:627-653.
61. Wang J, Mark S, Zhang X, Qian D, Yoo SJ, Radde-Gallwitz K, Zhang Y, Lin X, Collazo A, Wynshaw-Boris A, Chen P. 2005. Regulation of polarized extension and planar cell polarity in the cochlea by the vertebrate PCP pathway. Nat Genet 37:980-985.
62. Wang Y, Guo N, Nathans J. 2006. The role of Frizzled3 and Frizzled6 in neural tube closure and in the planar polarity of inner-ear sensory hair cells. J Neurosci 26:2147-2156.
63. Wu J, Mlodzik M. 2008. The frizzled extracellular domain is a ligand for Van Gogh/Stbm during nonautonomous planar cell polarity signaling. Dev Cell 15:462-469.
64. Yates LL, Dean CH. 2011. Planar polarity: a new player in both lung development and disease. Organogenesis 7:209-216.
65. Zhong Y, Zhu J, Wang Y, Zhou J, Ren K, Ding X, Zhang J. 2009. LIM domain protein TES changes its conformational states in different cellular compartments. Mol Cell Biochem 320:85-92.
66. Zhu J, Li X, Kong X, Moran MS, Su P, Haffty BG, Yang Q. 2012. Testin is a tumor suppressor and prognostic marker in breast cancer. Cancer Sci 103:2092-2101.